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Effect of the Intake of a Traditional Mexican Beverage Fermented with Lactic Acid Bacteria on Academic Stress in Medical Students

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Effect of the Intake of a Traditional Mexican Beverage Fermented with Lactic Acid Bacteria on Academic Stress in Medical Students nutrients Article Effect of the Intake of a Traditional Mexican Beverage Fermented with Lactic Acid Bacteria on Academic Stress in Medical Students Laura Márquez-Morales 1 , Elie G. El-Kassis 1 , Judith Cavazos-Arroyo 2 , Valeria Rocha-Rocha 1, Fidel Martínez-Gutiérrez 3 and Beatriz Pérez-Armendáriz 1,* 1 Biological Science Department, Universidad Popular Autónoma del Estado de Puebla, Puebla 72410, Mexico; [email protected] (L.M.-M.); [email protected] (E.G.E.-K.); [email protected] (V.R.-R.) 2 Social Science Department, Universidad Popular Autónoma del Estado de Puebla, Puebla 72410, Mexico; [email protected] 3 Center for Research in Health Sciences and Biomedicine, Faculty of Chemical Science, Universidad Autónoma de San Luis Potosí, San Luis Potosi 78290, Mexico; fi[email protected] * Correspondence: [email protected]; Tel.: +52-(222)-2299400 (ext. 7774) Abstract: Dysbiosis of the gut microbiota has been associated with different illnesses and emotional disorders such as stress. Traditional fermented foods that are rich in probiotics suggest modulation of dysbiosis, which protects against stress-induced disorders. The academic stress was evaluated in medical students using the SISCO Inventory of Academic Stress before and after ingestion of an aguamiel-based beverage fermented with Lactobacillus plantarum, Lactobacillus paracasei and Lactobacil- Citation: Márquez-Morales, L.; lus brevis (n = 27) and a control group (n = 18). In addition, microbial phyla in feces were quantified El-Kassis, E.G.; Cavazos-Arroyo, J.; by qPCR. The results showed that the consumption of 100 mL of a beverage fermented with lactic Rocha-Rocha, V.; Martínez-Gutiérrez, acid bacteria (3 × 108 cfu/mL) for 8 weeks significantly reduced academic stress (p = 0.001), while the F.; Pérez-Armendáriz, B. Effect of the Intake of a Traditional Mexican control group (placebo intervention) had no significant changes in the perception of academic stress Beverage Fermented with Lactic Acid (p = 0.607). Significant change (p = 0.001) was shown in the scores for environmental demands, and Bacteria on Academic Stress in physical and psychological factors. Consumption of the fermented beverage significantly increased Medical Students. Nutrients 2021, 13, the phyla Firmicutes and Bacteroidetes but not Gammaproteobacteria. No significant changes were 1551. https://doi.org/10.3390/ found in the control group, except for a slight increase in the phylum Firmicutes. The intake of this nu13051551 fermented beverage suggest a modulation of gut microbiota and possible reduction in stress-related symptoms in university students, without changing their lifestyle or diet. Academic Editor: Alessandra Bordoni Keywords: aguamiel; academic stress; lactic acid bacteria; dysbiosis; gut microbiota; medical students Received: 31 March 2021 Accepted: 26 April 2021 Published: 5 May 2021 1. Introduction Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in Various studies have shown that gut microbiota are linked to stress due to the constant, published maps and institutional affil- bidirectional communication on the microbiota–gut–brain axis [1–3]. However, the totality iations. of communication pathways has yet to be detected, which is a challenge for future studies. Synbiotics, probiotics and prebiotics appear to have the ability to modulate microbiota, which have a close relationship with axis communication and its effect on stress reduction. Gut microbiota are seen to be altered by stress and produce communication inconsis- tencies on the gut microbiota–brain axis when stress becomes chronic [4]. Experiencing Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. stress has been shown to release cortisol, which activates the hypothalamic–pituitary– This article is an open access article adrenal axis (HPA) [5]. The hypothalamus sends signals that activate the secretion of distributed under the terms and corticotropin releasing hormone (CRH), which, in turn, triggers the release of the adreno- conditions of the Creative Commons corticotropic hormone (ACTH) leading to the secretion of glucocorticoids in the adrenal Attribution (CC BY) license (https:// cortex [6]. As a result, norepinephrine and dopamine are released [7], causing an imbalance creativecommons.org/licenses/by/ in the composition of the gut microbiota and, with that, in the gut bacterial phyla, and 4.0/). neuronal alterations [8,9]. Nutrients 2021, 13, 1551. https://doi.org/10.3390/nu13051551 https://www.mdpi.com/journal/nutrients Nutrients 2021, 13, 1551 2 of 18 The gut microbiota can be defined as the community of microorganisms and viruses, whose concentration is estimated to be approximately in the order of 1013–1014 and which interact synbiotically in the human intestine [10–12]. Representative phyla of the gut microbiota include Firmicutes, Bacteroidetes, Proteobacteria, Actinobacteria, Archaea, Fu- sobacteria and Verrucomicrobiota [13–15]. Previous studies have shown that the genera Lactobacillus and Bifidobacteria, belonging to the phyla Firmicutes and Actinobacteria, re- spectively, are producers of gamma-aminobutiric acid and serotonin [16], both of which are altered in stressed individuals [17], causing dysbiosis characterized by the growth of enterobacteriaceae capable of producing norepinephrine [18,19]. This leads to a stress feedback loop. These bacterial changes in the gut microbiota can lead to depression and anxiety [20,21], impairment of memory and reasoning [22,23], sleep disorders [24] and irritable bowel syndrome [25], all of which have been detected in university students. In recent years, medical students have been reported to present particularly high stress levels due to being exposed to many academic demands [26–28]. Preclinical stud- ies have shown that stool samples, obtained from university students after a high-stress situation such as an examination period, evidenced a marked reduction in lactic acid mi- croorganisms [29,30] (Figure1). Another clinical study showed that subjects suffering from stress-related irritable bowel syndrome presented an increase in the phyla Proteobacteria and Barnesiella, but a decrease in Firmicutes and Bacteroidetes [31]. In addition, people in a state of depression—a mental illness that, on many occasions, presents in stressed students—showed an increase in Bacteroidetes, Proteobacteria and Actinobacteria and a decrease in Firmicutes [32]. In animal studies, dysbiosis has also been observed in gut microbiota when subjects were exposed to social disruption [33,34]. Recent studies have sought to restore balance to the gut microbiota through synbiotic foods that appear to have a beneficial effect on human health and the neuronal functions of the brain [35]. Synbiotics are a mix of probiotics and prebiotics. Probiotics are living microorganisms which, at the right dose, improve health. Prebiotics, in contrast, are substances which cannot be digested by the body, but which induce the growth and activity of probiotics [36]. Earlier studies of interventions with Lactobacillus casei Shirota probiotics have demon- strated a reduction in stress as well as favorable effects on intestinal dysfunction problems and changes in the microbial diversity of the gut [37]. Analysis of the consumption of the synbiotic Ecologic®825, which contains different strains of Lactobacillus and Bifidobacteria, evidenced changes in emotional memory, reasoning and emotional decision-making [38], abilities that are diminished under stress. Meanwhile, sleep quality and symptoms of anxiety and depression in stressed students were improved with the use of heat-activated Lactobacillus gasseri strain CP2305. Furthermore, an increase was shown in the genus Bifi- dobacterium, as well as a reduction in streptococci [39]. On the other hand, nine lyophilized strains of the genera Lactobacillus and Bifidobacterium, in the synbiotic Ecologic®Barrier, improve cognition in depressed university students, without reducing depression [40]. Recently, there has been a great interest in demonstrating the relationship of prebiotic and probiotic consumption on mental health, as shown in Table1. Previous studies have shown that traditional fermented foods are a good source of pro- biotics and prebiotics that can modulate the gut microbiota [48,49]. In Mexico, pulque, a pre- Hispanic millennial drink, is a good source of lactic acid bacteria (LAB) [50,51]. Aguamiel is rich in fiber, which acts as a prebiotic, and contains fructooligosaccharides—short polymers of fructose (inulin)—which promote the survival of probiotics in the colon [52]. Aguamiel can also help regulate the gut microbiota [53]. There are few studies of experimental inter- ventions with synbiotics made from products such as pulque and Aguamiel, particularly in stressed university students. Nutrients 2021, 13, x FOR PEER REVIEW 2 of 20 cotropin releasing hormone (CRH), which, in turn, triggers the release of the adrenocorti- cotropic hormone (ACTH) leading to the secretion of glucocorticoids in the adrenal cortex [6]. As a result, norepinephrine and dopamine are released [7], causing an imbalance in the composition of the gut microbiota and, with that, in the gut bacterial phyla, and neu- ronal alterations [8,9]. The gut microbiota can be defined as the community of microorganisms and viruses, whose concentration is estimated to be approximately in the order of 1013–1014 and which interact synbiotically in the human intestine [10–12]. Representative phyla of the gut mi- crobiota include
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